Rodentia: Diatomyidae) and Some Other Rock-Dwellers

Home , Ctenodactylus, Diatomyidae, Gundi

Russian J. Theriol. 13(2): 83–95 © RUSSIAN JOURNAL OF THERIOLOGY, 2014

Short muscles of the hand and foot in Laonastes aenigmamus (Rodentia: Diatomyidae) and some other rock-dwellers

Petr P. Gambaryan & Olga V. Zherebtsova*

ABSTRACT. The short muscles of the hand and foot in the relict rock rat Laonastes aenigmamus Jenkins et al., 2005 (Rodentia: Diatomyidae) were studied for the first time. Some other rock-dwellers, Ctenodac- tylus gundi, Chinchilla lanigera, Ochotona macrotis, as well as Ochotona dauurica, inhabiting the plain landscapes, were also included in the morphological analysis for comparative purposes. In spite of the different localities of pikas, the structure of the short muscles of the hand and foot in both species of Ochotona is practically identical. At the same time the pikas differ substantially from the investigated rodents by a number of features of the short muscles: by the absence of the mm. palmaris brevis and add. digiti secundi in the hand and m. abd. metatarsi V in the foot; by the absence of the typical mm. lumbricales in the hand and the whole absence of these muscles in the foot; by the presence only one belly of the m. abd. digiti quinti in the hand instead of two bellies in rodents. In all studied forms, the structure of the m. add. digiti quinti in the hand and the mm. interossei both in the hand and foot, are characterized by a great similarity. Among the three investigated rodents, the most essential differences of the short muscles are connected with the reduction of the first fingers in the hand and foot in Ctenodactylus and Chinchilla. It was indicated that in Laonastes the state of the mm. lumbricales is evidently the most primitive.

KEY WORDS: Chinchilla, Ctenodactylus, Laonastes, Ochotona, short muscles of the hand and foot.

Petr P. Gambaryan [[email protected]], Olga V. Zherebtsova [[email protected]], Zoological Institute of the Russian Academy of Sciences. Universitetskaya emb. 1, Saint Petersburg 199034, Russia. Короткие мышцы кисти и стопы у Laonastes aenigmamus (Rodentia: Diatomyidae) и некоторых других скальных обитателей

П.П. Гамбарян, О.В. Жеребцова

РЕЗЮМЕ. Впервые проведено изучение коротких мышц кисти и стопы у реликтовой скальной крысы Laonastes aenigmamus Jenkins et al., 2005 (Rodentia: Diatomyidae). В сравнительный морфоло- гический анализ включены и другие обитатели скал: Ctenodactylus gundi, Chinchilla lanigera, Ochotona macrotis так же, как и Ochotona dauurica, населяющая равнинные ландшафты. Несмотря на различ- ные местообитания пищух, строение коротких мышц кисти и стопы у двух видов Ochotona практи- чески идентично. В то же время по ряду особенностей коротких мышц пищухи существенно отличаются от исследованных грызунов: отсутствием mm. palmaris brevis и add. digiti secunda в кисти и m. abd. metatarsi V в стопе; отсутствием типичных mm. lumbricales в кисти и полным отсутствием этих мышц в стопе; наличием только одного брюшка m. abd. digiti quinti в кисти вместо двух у грызунов. У всех изученных форм строение m. adductor digiti quinti в кисти и mm. interossei как в кисти, так и в стопе характеризуется большим сходством. Наиболее существенные различия в строении коротких мышц у трех исследованных грызунов связаны с редукцией первых пальцев на кисти и стопе у Ctenodactylus и у Chinchilla. Показано, что у Laonastes состояние mm. lumbricales, по-видимому, наиболее примитивное.

КЛЮЧЕВЫЕ СЛОВА: Chinchilla, Ctenodactylus, Laonastes, Ochotona, короткие мышцы кисти и стопы.

Introduction lots of plants among the rocks that would dry out in open landscapes; second, it is easier to find cover from Recently described relict rodent Laonastes aenig- predators under the rock debris. It is quite possible that mamus Jenkins et al., 2005 (hereafter Laonastes) (Ro- Laonastes is capable of jumps from one stone to anoth- dentia: Diatomyidae) inhabits the rocky landscapes in er, rescuing from predators. In this connection, the Laos (Jenkins et al., 2005). These habitats are charac- short muscles of the hand and foot in Laonastes were terized by certain attractive conditions: first, there are studied to reveal the specific features of their structure * Corresponding author and work during the locomotion. 84 P.P. Gambaryan & O.V. Zherebtsova

Figure 1. The hand (left, A–D) from the volar side and the foot (left, A´–D´) from the plantar side: A, A´ — Laonastes aenigmamus; B, B´ — Ctenodactylus gundi; C, C´ — Chinchilla lanigera; D, D´ — Ochotona dauurica.

Ctenodactylus gundi Rothmann, 1776 (hereafter brought closer together with one or another of these Ctenodactylus) (Rodentia: Ctenodactylidae) from North groups by different authors (Jenkins et al., 2005; Daw- Africa, Chinchilla lanigera Bennett, 1829 (hereafter son et al., 2006; Huchon et al., 2007). At the same time Chinchilla) (Rodentia: Chinchillidae) from South Amer- Ochotona macrotis, in contrast with previous three ica, Ochotona macrotis Günther, 1875 (hereafter forms, is the representative of another order, Lagomor- Ochotona) (Lagomorpha: Ochotonidae) from Asia, as pha, though it is characterized by a similar size of body well as Laonastes, are rock dwelling forms and proba- and mode of life (Hoffmann & Smith, 2005). bly similar to him on their locomotor adaptations. There- In the structure of the hand and foot of the three fore, these animals were also included in the morpho- studied rodents there are a number of common features. logical analysis of the short muscles of the hand and First, the structure of their calluses, strongly protruding foot for comparison with Laonastes. Ochotona dauuri- on the volar side of the hand and the plantar side of the ca Pallas, 1776, inhabiting the plain landscapes, was foot, attracts the attention (Fig. 1A–C´). Besides finger also studied since for analysis of the adaptive special- calluses, the well developed pads are located at the ization both ecological forms of Ochotona must be bases of the hand claws. During the animals landing on considered. the stones, just these finger pads are apparently the first On the other side, at present Ctenodactylus and to touch the surface and keep the paws of rodents from Chinchilla belong to different infraorders, Ctenodacty- slipping. lomorphi and Hystricognathi, respectively (Dieterlen, In Ochotona, in contrast with investigated rodents, 2005; Woods & Kilpatrick, 2005). Laonastes was a principally different adaptation is observed. Its hands Short muscles of the hand and foot in Laonastes 85 and feet are covered by coarse hairs that similarly to like that in Ctenodactylus, is not developed. However, calluses prevents probably from slipping during the in Chinchilla, just like in Ctenodactylus, from this animals movement in the rocky landscapes (Fig. 1D, D´). thickening and from the internal surface of the callus A number of long and short muscles control the cover, the muscle bundles pass from right to left (Fig. movements of the hand and foot. Since the long mus- 2C). Besides, the muscle bundles (both the longitudinal cles were described separately (Gambaryan et al., 2013), to the first digit, and transversal in the thickness of the in this work, the descriptions of actually hand and foot medial callus) run from the prepollex, locating on the muscles and their comparative analysis were conduct- medial side of the hand. ed. The morphofunctional features of the short muscles In Ochotona, this muscle is absent. will be discussed in the next communication. M. abductor digiti quinti (Figs. 2–4). Besides two All studied forms of mammals are regarded in con- homologues of the m. palmaris brevis described above, cordance with the classification after Wilson and Reed- in all the three species of rodents, there is another er (2005). superficial muscle, locating deeper than the m. palmaris brevis. It originates by two independent bellies: one Material and methods goes from the distal edge of the prepollex, and the second belly begins from the top of the os pisiforme, Three species of Rodentia and two species of Lago- and both converge into a single tendon (Fig. 2A´, B´, morpha from the collections of the Zoological Institute C´). The latter is inserted on the proximal end of the of the Russian Academy of Sciences (ZIN, Saint Pe- lateral side of the first phalanx of digit V. tersburg) were investigated: the Laotian rock rat, Laon- In Ochotona, there is only one belly, going from the astes aenigmamus Jenkins et al., 2005 (n = 2; ZIN os pisiforme and terminating by two thin tendons (Figs. 99491, 99496); the gundi, Ctenodactylus gundi Roth- 3, 4D). To medial of them, the tendinous brunch ex- mann, 1776 (n = 1; ZIN 6641); the long-tailed chinchil- tends from the space between the fifth and fourth termi- la, Chinchilla lanigera Bennett, 1829 (n = 2; ZIN nal tendons of the m. fl. digitorum profundus. This 102069 (field numbers — 576a, 576b)); the Daurian brunch is apparently homologous to the mm. lumbri- pika, Ochotona dauurica Pallas, 1776 (n = 2; ZIN cales. In the result all three tendons fuse together over 102070 (262, 264)) and the large-eared pika, Ochotona the metacarpo–phalangeal sesamoids of digit V and macrotis Günther, 1875 (n = 1; ZIN 102071 (240)). form its typical perforating tendon. Adult specimens were preserved in 70º ethanol or 5% Mm. lumbricales (Figs. 2–4). In all the three spe- formalin. The short muscles of the hand and foot were cies of rodents, besides usual connection with the ten- examined with a binocular stereomicroscope Leica MZ6 don of the m. fl. digitorum profundus, these muscles using the total preparations. have more or less strong connection with the tendons of the m. fl. digitorum sublimis. In Laonastes, from the lateral side of a common Results plate of the m. fl. digitorum profundus, the muscle belly begins, which is also attached to the lateral tendon of Because the structure of the short muscles of the the m. fl. digitorum sublimis (Fig. 2A´). On the surface hand and foot in both species of pikas are identical, of the latter, two tendons are soon formed. One of them their descriptions are considered as common attribute is firmly linked to a common plate of the m. fl. digi- of the genus Ochotona. torum profundus, and the second tendon is inserted on the final tendon of the m. fl. digitorum sublimis to digit Short muscles of the hand IV from the medial side. These two tendons converge to the tectum above the metacarpo-phalangeal sesamoids M. palmaris brevis (Fig. 2). In Laonastes, there are of digit V, and bifurcate again under them. the well-developed prepollex and the os pisiforme. From A similar structure is observed in a typical final their surfaces, the muscle fibers, which are probably tendon of the m. fl. digitorum sublimis, which passes homologous to the m. palmaris brevis, originate and run under the tendon of the m. fl. digitorum profundus, to pads of the pulvini carpales (Fig. 2A). bifurcating over the metacarpo-phalangeal sesamoids. In Ctenodactylus, outside of all the actually hand Then these branches interflow again into a single ten- muscles, over the top of the os pisiforme there is a don, inserting on the plantar side of the proximal end of sesamoid. From its distal end, the first muscle bundle the second phalanx. goes to the inner surface of the skin of the proximal On the medial surface of the common plate and on lateral callus (Fig. 2B). From the medial side of the the tendon of the m. fl. digitorum profundus to the external fascia of final tendon of the m. flexor digi- second digit, there is the second muscle belly of the torum profundus, the muscle bundle comes to the sec- mm. lumbricales. Its final tendon is inserted on the ond proximal callus. It seems likely that these two superficial fascia, covering the tendon of the m. fl. independent muscles are homologous to the m. pal- digitorum profundus to digit II. Besides, three bellies of maris brevis. the actual mm. lumbricales originate in the interspaces In Chinchilla, above the os pisiforme, the thicken- between the tendons of the m. fl. digitorum profundus ing of the connective tissue is observed, but sesamoid, to digits II–III, III–IV, and IV–V, and are inserted on 86 P.P. Gambaryan & O.V. Zherebtsova Short muscles of the hand and foot in Laonastes 87

lateral part of the belly originates from the lateral side of a common plate of the m. fl. digitorum profundus. Simultaneously, it begins from the final tendon of the m. fl. digitorum sublimis to digit IV. Then this belly goes to the metacarpo-phalangeal sesamoids of digit V and terminates on it by a typical perforated tendon. In Ochotona, between the terminal tendons of the m. fl. digitorum profundus to digits IV and V, the tendon is only observed, which is probably homologous to the typical mm. lumbricales (Figs. 3, 4D). Mm. adductor digiti quinti and adductor digiti secundi (Fig. 4). In all the three rodents, the both muscles originate on the middle connective-tissue plate of the hand, and also on a common volar aponeurosis of all the mm. interossii. These muscles terminate on the proximal ends of the first phalanxes of digits V (from the medial side) and II (from the lateral side). In Ochotona, the origin and termination of the m. add. digiti quinti are the same as in investigated rodents but the m. add. digiti secundi is absent (Fig. 4D). Mm. abductor, flexor, and adductor pollicis brevis (Figs. 2, 4). In Laonastes, these three muscles interflow into a single muscle, which originates deeper than the m. abd. digiti quinti on the distal margin of the prepollex (Figs. 2A´, 4A). Its external fibers terminate on the medial edge of the first phalanx, and its lateral fibers insert on the lateral edge of same phalanx. The part of the longitudinal fibers reaches also the claw phalanx, inserting there under the tendon of the m. fl. digitorum profundus to the first digit. According their direction, the muscle bundles mentioned above can be conventionally divide into three muscles: abductor, adductor and flexor pollicis brevis, respectively. Figure 3. The muscles of the hand (left) from the volar side In Ctenodactylus, all these muscles are absent since (the superficial layer) in Ochotona dauurica. the first digit is rudimentary. In Chinchilla, the first finger is weaker developed than that in Laonastes, however there are all the three the fasciae, enveloping the tendons of the m. fl. digi- muscles, providing its mobility (Fig. 4C). torum profundus to digits II–IV. In Ochotona, there are only the m. fl. pollicis brevis In Ctenodactylus, after the removal of the m. pal- and the m. add. pollicis brevis (Fig. 4D). The tendon of maris brevis, two layers of the mm. lumbricales are the latter is inserted on the fasciae near the basis of the observed (Fig. 2B´). The first of them is related to the pulvinus digitalis. tendons of the m. fl. digitorum sublimis, and another is Mm. interossei (Fig. 4). In all studied rodents and connected with the tendons of the m. fl. digitorum Ochotona, there are eight these muscles: by two for profundus. In the first layer, the most powerful belly each of four lateral digits. M. interossei lateralis of digit originates a little distal to the level of the os pisiforme V begins on the distal surface of the os pisiforme. Other on the tendon of the m. fl. digitorum sublimis to digit V, muscles originate from a general volar aponeurosis and soon forms the perforating tendon. The second attached to the os carpalia, and on the volar surface of belly originates a little distal to the level of the os the metacarpales II–V. Mm. interossei terminate by pisiforme on the tendon of the m. fl. digitorum sublimis tendons that bypass the metacarpo-phalangeal sesam- to digit IV. The third belly is still in a quite rudimentary oids and are infused into the extensor tendons. Only in condition. It begins above the level of the os pisiforme Chinchilla, the m. interossei lateralis of the first digit is and terminates on the tendon of the m. fl. digitorum inserted on the metacarpo-phalangeal sesamoids, and it sublimis to digit II. is rather similar with the m. fl. pollicis brevis. In Chinchilla, the transformation of the mm. lum- In all investigated forms, the mm. interossei before bricales is a more advanced than that in Laonastes, but their insertions are infused into the tendons of the long is not so complex as in Ctenodactylus (Fig. 2C´). Most digit extensors (mm. extensor digitorum communis and

Figure 2. The muscles of the hand (left) from the volar side — the first, superficial (A´, B´, C´) and the second (A, B, C) layers: A, A´ — Laonastes aenigmamus; B, B´ — Ctenodactylus gundi; C, C´— Chinchilla lanigera. 88 P.P. Gambaryan & O.V. Zherebtsova

Figure 4. The muscles of the hand (left) from the volar side (the third layer): A — Laonastes aenigmamus; B — Ctenodactylus gundi; C — Chinchilla lanigera; D — Ochotona dauurica. Short muscles of the hand and foot in Laonastes 89 lateralis, and m. ext. pollicis longus). In Laonastes, lar abdomens appear, which terminate by their tendons, Chinchilla, and Ochotona, after the fusion, these ten- as well as the four perforating tendons. With these dons terminate directly on the proximal ends of the tendons from the surface, the flat tendons mentioned dorsal side of the second phalanxes of digits II–V. In above grow together. The muscular abdomens on the Ctenodactylus, these tendons are inserted on the sesam- internal surface of the described muscle are closely oids, which are also attached by a special cord to the related to the mm. lumbricales. same phalanx. From these sesamoids (or from the at- In Chinchilla, the muscle also completely trans- tachments of the extensor tendons on the second pha- forms into a tendinous plate. On the proximal half of its lanxes) the cords (ligamentum dorsalis) pass to the claw plantar surface, the pulvinus tarsalis is attached (Fig. phalanxes on both of their surfaces. 6C). Further, the tendon to the pulvinus metatarsalis of digit V separates, which also has a branch to the lateral Short muscles of the foot side of the proximal end of the first phalanx of digit V. Then three perforating tendons to digits II–IV separate, M. extensor digitorum brevis (Fig. 5). In Laonas- from which the tendinous retractors go to the pulvini tes and Ctenodactylus, it originates from the dorsal part metatarsales: one passes to digits IV-V, and the another of the distal end of the heel bone and runs by two — to digit II. Besides, from the total flexor tendon, the tendons to digits II and III (Fig. 5A, B). These tendons tendinous plates also go to the pulvinus metatarsalis of infuse in the appropriate tendons of the m. ext. digi- digit IV. torum longus, which terminate on special sesamoids in In Ochotona, this muscle, as an immediate continu- the joint capsules between the first and second phalanx- ation of the m. plantaris tendon, passes on the foot and es of digits II and III. The tendons of the mm. interossei forms a common tendinous plate (Fig. 6D). The latter approach from the right and left to the same sesamoids. divides into four typical perforating tendons, going to The very joint capsules thicken in front and particularly four digits. firmly attached to the dorsal part of the proximal end of M. quadratus plantae (Fig. 6). In Laonastes, it the second phalanxes. From the edge of these attach- originates on the latero-distal part of the plantar surface ments, a loose connective-tissue subcutaneous plate of the os calcaneus and inserts onto a common tendi- goes to the bases of the paries cornea, and the elastic nous plate of the mm. fl. digitorum fibularis and tibialis. cords (ligamentum dorsalis) pass to the bases of claw In Chinchilla, the origin of the muscle additionally phalanxes on both sides. extends on the lateral side of the proximal end of the In Chinchilla, the m. ext. digitorum brevis begins by Mt. V (Fig. 6C). Its insertion is like that in Laonastes. two separate abdomens located between the proximal In Ctenodactylus and Ochotona, this muscle is ab- ends of the Mt. V and IV, as well as the Mt. IV and III sent. (Fig. 5C). They terminate like those in the previous two Mm. lumbricales (Fig. 6). In Laonastes, the first species. abdomen of the muscle originates between the tendons In Ochotona, this muscle originates like that in of the m. fl. fibularis to the first and second digits (Fig. Laonastes and Ctenodactylus, however then it forms 6A). The tendon of the muscle goes to the medial three tendons, which pass from the deep to the terminal metatarso-phalangeal sesamoid and there merges with tendons of the m. ext. digitorum longus at the level of the tendon of the mm. interossei. The latter merges with metacarpo-phalangeal joints of digits II–IV (Fig. 5D). the tendon of the m. ext. digitorum longus onto the Their terminal insertions are the same as those in ro- inter-phalangeal sesamoid. The second and third abdo- dents. mens originate between the tendons of the m. fl. fibu- M. flexor digitorum brevis (Fig. 6). In Laonastes, laris to the second and third digits. The second abdo- the origin of this muscle presents the final tendon of the men inserts onto the tendon of the m. fl. digitorum m. plantaris (Fig. 6A). Further this tendon expands, and brevis to the third digit, and the third abdomen — onto at the level of the distal part of the first metatarsal callus the inter-phalangeal joint capsule from the medial side the muscle fibers are appeared on it. From the external and tendon of the mm. interossei. The fourth and fifth surface of these fibers, the tendinous retractors to the abdomens originate between the tendons of the m. fl. bases of the calluses (two pulvini carpales and three fibularis to the third and fourth digits, and insert like the pulvini metacarpales) separate. The muscular abdomen previous two abdomens. However, the sixth abdomen itself soon forms three perforating tendons to the three on digit IV originates on the lateral surface of the middle digits, which below the metatarso-phalangeal tendon of the m. fl. fibularis to digit V. It inserts as a sesamoids bifurcate. The muscle terminates under the typical perforating tendon, which bifurcates at the level tendons of the m. fl. digitorum fibularis on the plantar of the metatarso-phalangeal sesamoids and terminates surface of the proximal end of the second phalanxes of on the plantar side of the second phalanx of digit V. the respective digits II–IV. In Ctenodactylus, one muscle belly originates from In Ctenodactylus, the muscle completely transforms the medial side of a total plate of the mm. fl. digitorum into a tendinous plate, terminating by four flat tendons fibularis and tibialis at the level of the proximal ends of on the metatarso-phalangeal sesamoids (Fig. 6B). On the metatarsal bones (Fig. 6B). In the middle of this the internal surface of this plate, the four weak muscu- abdomen, the tendon of the second abdomen passes, the 90 P.P. Gambaryan & O.V. Zherebtsova Short muscles of the hand and foot in Laonastes 91 latter being originate on the dorsal surface of a tendi- on every digit except the first one, which is a rudimen- nous plate of the m. fl. digitorum brevis. These two tary digit in Ctenodactylus and is absent in Chinchilla abdomens terminate together in the inter-sesamoid space and Ochotona. Mm. interossei originate on both sides and form the perforating tendon of digit V. The other of the metatarsalia II–V, bypass the sesamoids, and three abdomens are arranged similarly and originate insert on the fused extensor tendons on the proximal from the edges of the tendons of the m. fl. digitorum ends of the second phalanxes of digits II–V. fibularis to digits III–V and a common tendinous plate. M. abductor, flexor, and adductor hallucis brevis Then they join with the tendons of the m. fl. digitorum (Fig. 7). In Laonastes, there are all the three muscles. brevis and insert as the typical perforating tendons. Mm. abductor and flexor hallucis brevis originate from In Chinchilla, there are three muscles located in the the internal surface of the prehallux and medial lip of bases of the tendons of the m. fl. digitorum fibularis the Mt. I, and terminate on the medio-proximal side of between the digits II–III, III–IV, and IV–V (Fig. 6C). the first phalanx of the first digit (Fig. 7A). M. add. Before the insertion, the terminal tendons of the first hallucis brevis originates from the midline of the sec- two muscles merge into the m. interossei medialis of ond metatarsal bone at the level of the proximal 2/3 of digits III–IV. The third abdomen inserts on the medial its length. The muscle inserts on the lateral side of the side of the plantar surface of the proximal end of the first phalanx of first digit. second phalanx of digit V. In this case, in contrast to In Ctenodactylus, there are only two muscles: mm. that in Laonastes and Ctenodactylus, the perforating flexor and adductor hallucis brevis, since the first digit tendons are not formed. is rudimentary (Fig. 7B). In Ochotona, these muscles are absent. In Chinchilla, all the three muscle, providing the Mm. adductor (indicis proprius) digiti secundi first digit mobility, are absent as a result of its whole and adductor digiti quinti (Fig. 7). In Laonastes, both reduction. In Ochotona, the same state is observed. muscles originate from the midline of the third metatarsal bone at the level of the proximal 2/3 of its length Conclusion (Fig. 7A). M. add. digiti secundi inserts on the lateral side of the first phalanx of digit II; the m. add. digiti The comparative morphological analysis revealed a quinti terminates on the medial side of the proximal end number of features in the structure of the short muscles of the first phalanx of digit V. of the hand in Ochotona, which differ from those in the In Ctenodactylus, the mm. adductors digiti secundi three forms of studied rodents: (1) the absence of the and digiti quinti originate at the base of digits III and IV mm. palmaris brevis and adductor digiti secundi; (2) by the thin tendons (Fig. 7B). They go to the proximal the absence of the typical mm. lumbricales and the ends of the first phalanxes: from the lateral side on digit availability instead of them a tendon, which is evidently II and from the medial side on digit V. homologous to these muscles; (3) the m. abductor digiti In Chinchilla, there are both muscles, but they are quinti originates from the os pisiforme by means of greatly weakened, and in the form of thin muscular only one belly instead of two bellies in rodents. films insert by the transparent tendons on the medial In the structure of the short muscles of the foot in side of the proximal end of the first phalanx of digit V Ochotona, such essential distinctions from rodents as (m. add. digiti quinti) and by the same way on the the absence of the mm. lumbricales and m. abd. meta- lateral side of digit II (m. add. digiti secundi) (Fig. 7C). tarsi V were revealed. It can be note also the formation In Ochotona, mm. add. digiti secundi and add. digiti of the three final tendons of the m. ext. digitorum brevis quinti, in compared with those of the previous forms, instead two of those in rodents. are stronger developed and originate from the midline The structure of the m. adductor digiti quinti in the of the pes plantar surface. Their insertions are the same hand and mm. interossei in both the hand and the foot as those of rodents (Fig. 7D). are characterized by a great similarity in all studied M. abductor metatarsi V (Fig. 7). In Laonastes forms, though in Ctenodactylus, the insertions of the and Ctenodactylus, it originates on the plantar surface mm. interossei in the hand in any way differ a little. of the calcaneal tuber and inserts on the latero-proximal In four investigated forms, in Ctenodactylus gundi, tuberculum of the Mt. V (Fig. 7A, B). Chinchilla lanigera, Ochotona macrotis and O. dauu- In Chinchilla, it is completely transformed into a rica, in the structure of the hand and foot, a common tendon, which begins from the medial surface of the tendency evidently connected with a similar locomotor calcaneal tuber and terminates on the lateral surface of adaptation to the rock landscapes, can be noted. In the the proximal end of the Mt. V. result of the first digit reduction, the narrowing of the In Ochotona, this muscle is absent. hand and foot are observed. With this connection it can Mm. interossei (Figs. 5, 7). In Laonastes, there are be suggested that the adaptation to the plain landscapes ten muscles: by two muscles on every digit. In all other in Ochotona was the secondary phenomenon. It should studied forms, there are eight muscles: by two muscles be emphasized that in studied forms the tendency men-

Figure 5. The pes muscles (left) from the dorsal side: A — Laonastes aenigmamus; B — Ctenodactylus gundi; C — Chinchilla lanigera; D — Ochotona dauurica. 92 P.P. Gambaryan & O.V. Zherebtsova Short muscles of the hand and foot in Laonastes 93 tioned above is expressed in different extent. In the sublimis. This belly terminates as a typical perforating hand the reduction of the first digit is most manifested tendon, simulating the fourth tendon of the m. fl. digi- in Ctenodactylus, and the same in the foot structure — torum sublimis to digit V. In primates, the m. fl. digi- in Chinchilla and Ochotona. In Laonastes, there are torum sublimis has four or, more seldom, five its own valuable five-fingers states of the hand and foot. There- final tendons. Apparently, the lateral and medial ten- fore, the latter can be probably considered as relict dons of the m. fl. digitorum sublimis in primates are rodent, which is most close to the level of the morpho- derivatives of the mm. lumbricales. logical specialization of the ancestor form for Cteno- Besides, Laonastes differs from other two rodents hystrica (Huchon et al., 2007). by the region of the origin of the mm. adductors digiti The results of the comparative analysis of the short secundi and digiti quinti, m. fl. digitorum brevis in the muscles confirm to the conclusion mentioned above. foot. The latter in Laonastes forms three final tendons The one of the most essential differences in the hand instead four of those in Ctenodactylus and Chinchilla. and foot structure is manifested in respect of the mus- In regard to other short muscles of the foot, it is cles, responsible for the mobility of the first digits. necessary to note a similar structure of the m. abductor Among investigated forms, Laonastes is notable by the metatarsi V in Laonastes and Ctenodactylus. In Chin- presence of a whole set of these muscles: mm. abductor, chilla, this muscle is transformed completely into a flexor and adductor pollicis brevis in the hand, and mm. tendon, and in Ochotona, it is absent. A greater similar- abductor, flexor and adductor hallucis brevis in the ity between Laonastes and Ctenodactylus is also ob- foot. However, it is necessary to note a single undiffer- served in region of the initial attachment of the m. ext. entiated origin of these muscles in its hand. digitorum brevis and formation of the perforating ten- In Ctenodactylus, the first digit of the hand is rudi- dons of the mm. lumbricales. In Chinchilla, such ten- mentary, and all the three muscles, providing its mobil- dons are not formed. At the same time the development ity, are absent. In the foot, the first digit is weakly of the m. quadratus plantae is a common feature of developed, and there are only mm. flexor and adductor Laonastes and Chinchilla, and, on the contrary, its ab- hallucis brevis. sence is characteristic of Ctenodactylus and Ochotona. In Chinchilla, the first digit in the hand is weaker The wide discussion of all revealed features of the developed than that in Laonastes, but there are all the short muscles of the hand and foot in the three studied three muscles responsible for its mobility. In the foot, forms of rodents and Ochotona will be planned in the on the contrary, the all muscles of the first digit are next communication on the base of the new morpho- absent with the connection of its whole reduction. In functional data received. Ochotona, the very similar state is observed, however in the hand the m. abductor pollicis brevis is absent. ACKNOWLEDGEMENTS. The authors would like Among the studied rodents, the m. abductor digiti to thank Dr. Alexei V. Abramov (ZIN of RAS, Saint quinti in the hand is characterized by a great similarity, Petersburg) for the opportunity to examine the unique but the structure of the m. palmaris brevis, on the material on Laonastes aenigmamus collected in Laos. contrary, varies. Special thanks to Vladimir V. Platonov for help in the In regard to the mm. lumbricales of the hand, the work with figures and “American Journal Experts” for most simple and probably the most primitive their struc- the correction of English. We are especially grateful to ture is observed in Laonastes. In contrast to that, the Dr. Elena G. Potapova (IPEE of RAS, Moscow) and most advanced state of these muscles is noted in Cteno- Dr. Yuri F. Ivlev (IPEE of RAS, Moscow) for review- dactylus; Chinchilla in this relation takes an intermedi- ing the manuscript and constructive recommendations. ate position. The study was supported by Russian Foundation for The data obtained on the topography and attach- Basic Research (grant No 10-04-00973). ment of the lateral belly of the mm. lumbricales in the hand, allow us to follow one of the developmental paths References of the forth final tendon of the m. fl. digitorum sublimis in rodents. The matter is that in the majority of marsupi- Dawson M.R., Marivaux L., Li Ch., Beard K.Ch. & Metais als, rodents, and insectivores, the m. fl. digitorum subli- G. 2006. Laonastes and the “Lazarus effect” in recent mis has three final tendons, terminating on the three mammals // Science. Vol.311. P.1456–1458. middle digits (Dobson, 1882; Parsons, 1894, 1898; Dieterlen F. 2005. Suborder Hystricomorpha. Infraorder Cten- Howell, 1926; Green, 1935; Reed, 1951; Rinker, 1954; odactylomorphi // Wilson D.E. & Reeder D.M. (eds.). Gambaryan, 1960; Jullien, 1967; Jouffroy, 1971; Mammal Species of the World. A Taxonomic and Geo- Zherebtsova, 2001). In all investigated rodents, the graphic Reference. Third edition. Vol.2. Baltimore: Johns fourth tendon as derivative of the mm. lumbricales Hopkins University Press. P.1536–1537. appears. Their separate belly is closely associated with Dobson G.E. 1882. A Monograph of the Insectivora, Sys- a common tendinous plate of the m. fl. digitorum pro- tematic and Anatomical. Pt. I. London: John van Voorst. fundus and the lateral tendon of the m. fl. digitorum 172 p.

Figure 6. The pes muscles (left) from the plantar side (the superficial layer): A — Laonastes aenigmamus; B — Ctenodactylus gundi; C — Chinchilla lanigera; D — Ochotona dauurica. 94 P.P. Gambaryan & O.V. Zherebtsova Short muscles of the hand and foot in Laonastes 95

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Figure 7. The pes muscles (left) from the plantar side (the deep layer): A — Laonastes aenigmamus; B — Ctenodactylus gundi; C — Chinchilla lanigera; D — Ochotona dauurica.